Expression patterns in alternative splicing forms of prosaposin mRNA in the rat facial nerve nucleus after facial nerve transection

Neuroscience Research

Volumn 60, Issue 1, 2008, Pages 82-94

  Chen, Jie ^a   Saito, Shouichiro ^b   Kobayashi, Naoto ^a   Sato, Kohji ^c   Terashita, Takehiro ^a   Shimokawa, Tetsuya ^a   Mominoki, Katsumi ^d   Miyawaki, Kyojy ^e   Sano, Akira ^f   Matsuda, Seiji ^a  

^a EHIME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b GIFU UNIVERSITY   (Japan)

^c HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d EHIME UNIVERSITY   (Japan)

^e EHIME UNIVERSITY   (Japan)

^f KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

Facial nerve nucleus; In situ hybridization; Microglia; Neuroregeneration; Neurotrophic factor; Saposin B

Indexed keywords

HYDROLASE; MESSENGER RNA; NEUROTROPHIC FACTOR; PROLINE; PROSAPOSIN; PROTEIN PRECURSOR; SAPOSIN A; SAPOSIN B; SAPOSIN C; SAPOSIN D; SPHINGOLIPID ACTIVATOR PROTEIN; SPHINGOLIPID HYDROLASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; FACIAL NERVE NUCLEUS; GENE EXPRESSION; GENE INSERTION; LYSOSOME; MALE; MICROGLIA; MOTONEURON; NERVE REGENERATION; NERVE TRANSECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RAT; RNA SPLICING;

ALTERNATIVE SPLICING; ANIMALS; DENERVATION; FACIAL NERVE; FACIAL NERVE INJURIES; GENE EXPRESSION REGULATION; MALE; MICROGLIA; MOTOR NEURONS; NERVE REGENERATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHOMBENCEPHALON; RNA, MESSENGER; SAPOSINS; UP-REGULATION;

EID: 37549026431     PISSN: 01680102     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neures.2007.09.010     Document Type: Article

References (58)

1. Barron K.D., Marciano F.F., Amundson R., and Mankes R. Perineuronal glial responses after axotomy of central and peripheral axons. A comparison. Brain Res. 523 (1990) 219-229
2. Batchelor P.E., Porritt M.J., Martinello P., Parish C.L., Liberatore G.T., Donnan G.A., and Howells D.W. Macrophages and microglia produce local trophic gradients that stimulate axonal sprouting toward but not beyond the wound edge. Mol. Cell. Neurosci. 21 (2002) 436-453
3. Calcutt N.A., Campana W.M., Eskeland N.L., Mohiuddin L., Dines K.C., Mizisin A.P., and O'Brien J.S. Prosaposin gene expression and the efficacy of a prosaposin-derived peptide in preventing structural and functional disorders of peripheral nerve in diabetic rats. J. Neuropathol. Exp. Neurol. 58 (1999) 628-636
4. Campana W.M., Hiraiwa M., and O'Brien J.S. Prosapotide activates the MAPK pathway by a G-protein-dependent mechanism essential for enhanced sulfatide synthesis by Schwann cells. FASEB J. 12 (1998) 307-314
5. Campana W.M., Mohiuddin L., Misasi R., O'Brien J.S., and Calcutt N.A. Prosaposin-derived peptides enhanced sprouting of sensory neurons in vitro and induced sprouting at motor endplates in vivo. J. Peripher. Nerv. Syst. 5 (2000) 126-130
6. Che Y.H., Tamatani M., and Tohyama M. Changes in mRNA for post-synaptic density-95 (PSD-95) and carboxy-terminal PDZ ligand of neuronal nitric oxide synthase following facial nerve transection. Mol. Brain Res. 76 (2000) 325-335
7. Cohen T., Ravid L., Altman N., Madar-Shapiro L., Fein A., Weil M., and Horowitz M. Conservation of expression and alternative splicing in the prosaposin gene. Mol. Brain Res. 129 (2004) 8-19
8. Cohen T., Auerbach W., Ravid L., Bodennec J., Fein A., Futerman A.H., Joyner A.L., and Horowitz M. The exon 8-containing prosaposin gene splice variant is dispensable for mouse development, lysosomal function, and secretion. Mol. Cell Biol. 25 (2005) 2431-2440
9. Collard M.W., Sylvester S.R., Tsuruta J.K., and Griswold M.D. Biosynthesis and molecular cloning of sulfated glycoprotein 1 secreted by rat Sertoli cells: sequence similarity with the 70-kilodalton precursor to sulfatide/GM1 activator. Biochemistry 27 (1988) 4557-4564
10. Dai C.F., Kanoh N., Li K.Y., and Wang Z. Study on facial motoneuronal death after proximal or distal facial nerve transection. Am. J. Otol. 21 (2000) 115-118
11. Elkabes S., DiCicco-Bloom E.M., and Black I.B. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J. Neurosci. 16 (1996) 2508-2521
12. Fu Q., Carson G.S., Hiraiwa M., Grafe M., Kishimoto Y., and O'Brien J.S. Occurrence of prosaposin as a neuronal surface membrane component. J. Mol. Neurosci. 5 (1994) 59-67
13. Gillen C., Gleichmann M., Spreyer P., and Muller H.W. Differentially expressed genes after peripheral nerve injury. J. Neurosci. Res. 42 (1995) 159-171
14. Graeber M.B., Streit W.J., and Kreutzberg G.W. Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J. Neurosci. Res. 21 (1988) 18-24
15. Henseler M., Klein A., Glombitza G.J., Suziki K., and Sandhoff K. Expression of the three alternative forms of the sphingolipid activator protein precursor in baby hamster kidney cells and functional assays in a cell culture system. J. Biol. Chem. 271 (1996) 8416-8423
16. Hineno T., Sano A., Kondoh K., Ueno S., Kakimoto Y., and Yoshida K. Secretion of sphingolipid hydrolase activator precursor, prosaposin. Biochem. Biophys. Res. Commun. 176 (1991) 668-674
17. Hiraiwa M., O'Brien J.S., Kishimoto Y., Galdzicka M., Fluharty A.L., Ginns E.I., and Martin B.M. Isolation, characterization, and proteolysis of human prosaposin, the precursor of saposins (sphingolipid activator proteins). Arch. Biochem. Biophys. 304 (1993) 110-116
18. Hiraiwa M., Campana W.M., Martin B.M., and O'Brien J.S. Prosaposin receptor: evidence for a G-protein-associated receptor. Biochem. Biophys. Res. Commun. 240 (1997) 415-418
19. Hiraiwa M., Taylor E.M., Campana W.M., Darin S.J., and O'Brien J.S. Cell death prevention, mitogen-activated protein kinase stimulation, and increased sulfatide concentrations in Schwann cells and oligodendrocytes by prosaposin and prosaptides. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 4778-4781
20. Hiraiwa M., Campana W.M., Mizisin A.P., Mohiuddin L., and O'Brien J.S. Prosaposin: a myelinotrophic protein that promotes expression of myelin constituents and is secreted after nerve injury. Glia 26 (1999) 353-360
21. Hiraiwa M., Liu J., Lu A.G., Wang C.Y., Misasi R., Yamauchi T., Hozumi I., Inuzuka T., and O'Brien J.S. Regulation of gene expression in response to brain injury: enhanced expression and alternative splicing of rat prosaposin (SGP-1) mRNA in injured brain. J. Neurotrauma 20 (2003) 755-765
22. Holtschmidt H., Sandhoff K., Furst W., Kwon H.Y., Schnabel D., and Suzuki K. The organization of the gene for the human cerebroside sulfate activator protein. FEBS Lett. 280 (1991) 267-270
23. Holtschmidt H., Sandhoff K., Kwon H.Y., Harzer K., Nakano T., and Suzuki K. Sulfatide activator protein. Alternative splicing that generates three mRNAs and a newly found mutation responsible for a clinical disease. J. Biol. Chem. 266 (1991) 7556-7560
24. Kawamoto M., Ohno K., Kuriyama K., Kubo T., and Sato K. Developmental changes in GABA transporter (GAT1 and GAT3) mRNA expression in the rat olfactory bulb. Dev. Brain Res. 126 (2001) 137-145
25. Kishimoto Y., Hiraiwa M., and O'Brien J.S. Saposins: structure, function, distribution, and molecular genetics. J. Lipid Res. 33 (1992) 1255-1267
26. Kondoh K., Sano A., Kakimoto Y., Matsuda S., and Sakanaka M. Distribution of prosaposin-like immunoreactivity in rat brain. J. Comp. Neurol. 334 (1993) 590-602
27. Kotani Y., Matsuda S., Sakanaka M., Kondoh K., Ueno S., and Sano A. Prosaposin facilitates sciatic nerve regeneration in vivo. J. Neurochem. 66 (1996) 2019-2025
28. Kotani Y., Matsuda S., Wen T.C., Sakanaka M., Tanaka J., Maeda N., Kondoh K., Ueno S., and Sano A. A hydrophilic peptide comprising 18 amino acid residues of the prosaposin sequence has neurotrophic activity in vitro and in vivo. J. Neurochem. 66 (1996) 2197-2200
29. Lamontagne S., and Potier M. Modulation of human saposin B sphingolipid-binding specificity by alternative splicing. A study with saposin B-derived synthetic peptides. J. Biol. Chem. 269 (1994) 20528-20532
30. Lefrancois S., Michaud L., Potier M., Igdoura S., and Morales C.R. Role of sphingolipids in the transport of prosaposin to the lysosomes. J. Lipid Res. 40 (1999) 1593-1603
31. Lind D., Franken S., Kappler J., Jankowski J., and Schilling K. Characterization of the neuronal marker NeuN as a multiple phosphorylated antigen with discrete subcellular localization. J. Neurosci. Res. 79 (2005) 295-302
32. Madar-Shapiro L., Pasmanik-Chor M., Vaccaro A.M., Dinur T., Dagan A., Gatt S., and Horowitz M. Importance of splicing for prosaposin sorting. Biochem. J. 337 (1999) 433-443
33. Mallat M., Houlgatte R., Brachet P., and Prochiantz A. Lipopolysaccharide-stimulated rat brain macrophages release NGF in vitro. Dev. Biol. 133 (1989) 309-311
34. McPhail L.T., McBride C.B., McGraw J., Steeves J.D., and Tetzlaff W. Axotomy abolishes NeuN expression in facial but not rubrospinal neurons. Exp. Neurol. 185 (2004) 182-190
35. Misasi R., Sorice M., Garofalo T., Griggi T., Campana W.M., Giammatteo M., Pavan A., Hiraiwa M., Pontieri G.M., and O'Brien J.S. Colocalization and complex formation between prosaposin and monosialoganglioside GM3 in neural cells. J. Neurochem. 71 (1998) 2313-2321
36. Nakajima K., Tohyama Y., Kohsaka S., and Kurihara T. Ceramide activates microglia to enhance the production/secretion of brain-derived neurotrophic factor (BDNF) without induction of deleterious factors in vitro. J. Neurochem. 80 (2002) 697-705
37. Nakano T., Sandhoff K., Stumper J., Christomanou H., and Suzuki K. Structure of full-length cDNA coding for sulfatide activator, a Co-beta-glucosidase and two other homologous proteins: two alternate forms of the sulfatide activator. J. Biochem. 105 (1989) 152-154
38. Nishimura M., Sato K., Mizuno M., Yoshida I., Shimada S., Saito N., and Tohyama M. Differential expression patterns of GABA transporters (GAT1-3) in the rat olfactory bulb. Mol. Brain Res. 45 (1997) 268-274
39. O'Brien J.S., and Kishimoto Y. Saposin proteins: structure, function, and role in human lysosomal storage disorders. FASEB J. 5 (1991) 301-308
40. O'Brien J.S., Kretz K.A., Dewji N., Wenger D.A., Esch F., and Fluharty A.L. Coding of two sphingolipid activator proteins (SAP-1 and SAP-2) by same genetic locus. Science 241 (1988) 1098-1101
41. O'Brien J.S., Carson G.S., Seo H.C., Hiraiwa M., and Kishimoto Y. Identification of prosaposin as a neurotrophic factor. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 9593-9596
42. O'Brien J.S., Carson G.S., Seo H.C., Hiraiwa M., Weiler S., Tomich J.M., Barranger J.A., Kahn M., Azuma N., and Kishimoto Y. Identification of the neurotrophic factor sequence of prosaposin. FASEB J. 9 (1995) 681-685
43. Sano A., Hineno T., Mizuno T., Kondoh K., Ueno S., Kakimoto Y., and Inui K. Sphingolipid hydrolase activator proteins and their precursors. Biochem. Biophys. Res. Commun. 165 (1989) 1191-1197
44. Sano A., Matsuda S., Wen T.C., Kotani Y., Kondoh K., Ueno S., Kakimoto Y., Yoshimura H., and Sakanaka M. Protection by prosaposin against ischemia-induced learning disability and neuronal loss. Biochem. Biophys. Res. Commun. 204 (1994) 994-1000
45. Sato K., and Tohyama M. Assessment of distribution of cloned ion channels in neuronal tissues. Methods Enzymol. 293 (1998) 155-165
46. Sikora J., Harzer K., and Elleder M. Neurolysosomal pathology in human prosaposin deficiency suggests essential neurotrophic function of prosaposin. Acta Neuropathol. 113 (2007) 163-175
47. Streit W.J. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40 (2002) 133-139
48. Streit W.J., and Kreutzberg G.W. Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J. Comp. Neurol. 268 (1988) 248-263
49. Streit W.J., Walter S.A., and Pennell N.A. Reactive microgliosis. Prog. Neurobiol. 57 (1999) 563-581
50. Terashita T., Saito S., Miyawaki K., Hyodo M., Kobayashi N., Shimokawa T., Saito K., Matsuda S., and Gyo K. Localization of prosaposin in rat cochlea. Neurosci. Res. 57 (2007) 372-378
51. Tseng G.F., Wang Y.J., and Lai Q.C. Perineuronal microglial reactivity following proximal and distal axotomy of rat rubrospinal neurons. Brain Res. 715 (1996) 32-43
52. Tsuboi K., Hiraiwa M., and O'Brien J.S. Prosaposin prevents programmed cell death of rat cerebellar granule neurons in culture. Dev. Brain Res. 110 (1998) 249-255
53. Unuma K., Chen J., Saito S., Kobayashi N., Sato K., Saito K., Wakisaka H., Mominoki K., Sano A., and Matsuda S. Changes in expression of prosaposin in the rat facial nerve nucleus after facial nerve transection. Neurosci. Res. 52 (2005) 220-227
54. Van Den Berghe L., Sainton K., Gogat K., Marchant D., Dufour E., Bonnel S., Gadin S., Menasche A., and Abitbol M. Prosaposin gene expression in normal and dystrophic RCS rat retina. Invest. Ophthalmol. Vis. Sci. 45 (2004) 1297-1305
55. Veilhaber G., Hurwitz R., and Sandhoff K. Biosynthesis, processing, and targeting of sphingolipid activator protein (SAP) precursor in cultured human fibroblasts. Mannose 6-phosphate receptor-independent endocytosis of SAP precursor. J. Biol. Chem. 271 (1996) 32438-32446
56. Yan L., Otero D.A., Hiraiwa M., and O'Brien J.S. Prosapotide D5 reverses hyperalgesia: inhibition of calcium channels through a pertussis toxin-sensitive G-protein mechanism in the rat. Neurosci. Lett. 278 (2000) 120-122
57. Yokota N., Uchijima M., Nishizawa S., Namba H., and Koide Y. Identification of differentially expressed genes in rat hippocampus after transient global cerebral ischemia using subtractive cDNA cloning based on polymerase chain reaction. Stroke 32 (2001) 168-174
58. Zhao Q., Bell A.W., El-Alfy M., and Morales C.R. Mouse testicular sulfated glycoprotein-1: sequence analysis of the common backbone structure of prosaposins. J. Androl. 19 (1998) 165-174